Diverse phylogeny and morphology of magnetite biomineralized by magnetotactic cocci

Abstract

Summary Magnetotactic bacteria (MTB) are diverse prokaryotes that produce magnetic nanocrystals within intracellular membranes (magnetosomes). Here, we present a large‐scale analysis of diversity and magnetosome biomineralization in modern magnetotactic cocci, which are the most abundant MTB morphotypes in nature. Nineteen novel magnetotactic cocci species are identified phylogenetically and structurally at the single‐cell level. Phylogenetic analysis demonstrates that the cocci cluster into an independent branch from other Alphaproteobacteria MTB, that is, within the Etaproteobacteria class in the Proteobacteria phylum. Statistical analysis reveals species‐specific biomineralization of magnetosomal magnetite morphologies. This further confirms that magnetosome biomineralization is controlled strictly by the MTB cell and differs among species or strains. The post‐mortem remains of MTB are often preserved as magnetofossils within sediments or sedimentary rocks, yet paleobiological and geological interpretation of their fossil record remains challenging. Our results indicate that magnetofossil morphology could be a promising proxy for retrieving paleobiological information about ancient MTB.

Biomineralization and Magnetism of Uncultured Magnetotactic Coccus Strain THC‐1 With Non‐chained Magnetosomal Magnetite Nanoparticles

“…However, morphological differences in particle size, elongation (aspect ratio), and crystal face area are observed clearly within elongated prismatic magnetite produced by different MTB species/strains (Li et al, 2017;Liu et al, 2020;Meldrum et al, 1993aMeldrum et al, , 1993bPósfai et al, 2013;this study). This further confirms that magnetite biomineralization within magnetosomes is genetically controlled and, therefore, species/strain specific (Li, Menguy, et al, 2020;Liu et al, 2020;Pósfai et al, 2013).…”

“…MTB are affiliated phylogenetically with the Alphaproteobacteria, Deltaproteobacteria, Gammaproteobacteria, and Etaproteobacteria classes of the Proteobacteria phylum, the Nitrospirae and candidate Omnitrophica (previously known as candidate division OP3) phyla, and even in other Bacterial lineages (Kolinko et al, 2016; Lefèvre & Bazylinski, 2013; Lin et al, 2018; Liu et al, 2020). Consistent with their bacterial diversity, biomineralization within MTB is diverse in terms of the number, size, morphology, and spatial assembly of magnetite crystals (Lefèvre & Bazylinski, 2013; Li, Menguy, et al, 2020; Liu et al, 2020; Pósfai et al, 2013). Studying the biomineralization and magnetism of magnetic particles produced by modern MTB can provide mineralogical and physical evidence to better understand the process and mechanisms of BCM and magnetotaxis in the MTB system (e.g., Li, Benzerara, et al, 2013; Li et al, 2015; Pósfai & Dunin‐Borkowski, 2009).…”

“…Based on morphological, crystallographic, magnetic, and chemical evidence, criteria or approaches have been proposed for identifying magnetofossils from sediments or rocks (e.g., Amor et al, 2015; Arató et al, 2005; Chang et al, 2016; Egli, 2004; Egli et al, 2010; Gehring et al, 2011, 2013; Kind et al, 2011; Li et al, 2012; Moskowitz et al, 1993; Thomas‐Keprta et al, 2000; Weiss et al, 2004). Although widely used, some of these criteria or approaches need to be reassessed because the crystal morphologies and arrangements of magnetosomal magnetic particles within modern MTB are diverse (e.g., Li, Benzerara, et al, 2013; Li, Menguy, et al, 2020; Liu et al, 2020; Pósfai et al, 2013), and spatial arrangements and/or chemical compositions of magnetofossils within the geological record may be altered during burial (e.g., Kopp & Kirschvink, 2008; Li et al, 2012; Li, Benzerara, et al, 2013; Roberts et al, 2013; Rodelli et al, 2019; Tarduno et al, 1998). Documenting bacterial diversity and biomineralization and magnetism of magnetosomal magnetic nanoparticles within modern MTB is, therefore, crucial for understanding the magnetofossil record.…”

“…Twenty novel magnetotactic cocci strains were identified phylogenetically and structurally at the single‐cell level (Liu et al, 2020; Zhang et al, 2017). Phylogenetic analysis demonstrates that the magnetotactic cocci cluster into the Etaproteobacteria class in the Proteobacteria phylum rather than the Alphaproteobacteria class (Liu et al, 2020). Transmission electron microscope (TEM) observations demonstrated that magnetosomes within these magnetotactic cocci are highly diverse in terms of chain configuration and crystal morphology.…”

“…Transmission electron microscope (TEM) observations demonstrated that magnetosomes within these magnetotactic cocci are highly diverse in terms of chain configuration and crystal morphology. Based on the spatial arrangement of magnetosome crystals, four groups of magnetotactic cocci were identified: single chain (six strains), double‐separated chains (five strains), two double chains (three strains), and nonlinear single or multiple chains (e.g., dispersed aggregates) (four strains), dispersed aggregates and partial chains (one strain), and partial clusters and partial chains (one strain) (Liu et al, 2020). Among these uncultured magnetotactic cocci, strain THC‐1 is interesting because it forms magnetosomal magnetite particles that are dispersed rather than being arranged into a chain structure.…”